Title: Elevated Mortality among Birds in Chernobyl as Judged from Skewed Age and Sex Ratios
Source: PLoS ONE Journal
Authors: Anders Pape Møller, Andrea Bonisoli-Alquati, Geir Rudolfsen, Timothy A. Mousseau
Date Published: April 11, 2012
Emphasis Added

[...] Here we extended this result by testing for a reduction in adult survival rate among 16 species of birds. Using age ratios of captured birds, we showed a reduction in adult survival rate by 40% in contaminated areas, but no difference between observed and expected adult survival rates based on Western European estimates when analyzing age ratios from uncontaminated areas in Ukraine. The estimated reduction in adult survival rate of barn swallows was 43%, similar to the value of 40% that we have previously reported based on capture-mark-recapture analyses [6]. We could exclude the possibility that this difference was caused by permanent emigration as shown by an absence of breeding dispersal among sites, and by no sex difference in the frequency of abnormalities between sites with normal and with higher levels of contamination. Although the conservation consequences of the Chernobyl disaster, and more recently the Fukushima disaster, are poorly known, they include reductions in the distribution and abundance of rare species and increases in the frequency of selective deaths due to mutations [29]. We can now start making estimates of the conservation implications of radiation exposure using adult survival rates as estimated from age ratios from the field for a large number of bird species. First, we know that populations in contaminated areas are maintained through immigration from source populations, because local reproduction and survival are insufficient for maintenance of stable populations [30]. Second, we have shown reduced adult survival rates [6; this study] and reproductive rates [6], [11] in contaminated areas. Age ratios for birds at normal and high background radiation levels differed considerably from an average of 43% at normal levels to an average of 73% at high levels. This observed difference in age ratios between control and contaminated areas implies an increase in the frequency of juveniles from 43% to 73%, or an increase by 30% (73% – 43%). Given that the area contaminated by more than 0.05 µSv/h exceeds 30,000 km2 (Fig. 1; [31]), and given that the typical population density of breeding birds exceeds 100 pairs per km2 [24], this implies an annual excess mortality of 30,000 km2 × 100 pairs/km2 × 0.3 = 1.8 million birds. These findings also imply that the magnitude of this ecological sink is likely to exceed that of any other sinks described in the literature (review in [32]). Therefore, the findings reported here also have significant conservation consequences caused by the Chernobyl disaster. Finally, skewed sex ratios may increase the risk of local extinction for demographic reasons [33], [34].

Female barn swallows suffer differentially from the mortality costs of radiation, with male adult survival being reduced by 24%, while female survival is reduced by 57% in contaminated areas compared to controls [6]. Thus differential mortality of females in contaminated areas, as shown for the barn swallow [6], causes male-skewed tertiary sex ratios. If such sex differences in survival rate were common, we should expect sex ratios among adults to be skewed towards males. Here we have reported such a skew across a large number of species, using captures of adult birds during the main breeding season, with the sex ratio increasing from parity at normal background radiation to more than 73% males at the highest radiation levels. We can exclude the possibility that these estimates were biased because we used mist netting to obtain samples of birds for sexing and aging. Mist netting is a reliable tool for research due to low observer bias, high detection probability of species that are often missed using other survey methods and ease of standardized sampling [35]. The hypothesis of differential mortality in female birds due to greater expenditure of antioxidants [8] as a cause of male-skewed sex ratios is also consistent with the observation that bird species in which females invest the most in production of eggs through maternal allocation of antioxidants to eggs are the species that experience the strongest reduction in abundance of breeding birds due to radiation [18].

Birds sing to attract mates and repel potential competitors [12]. We have shown here that the fraction of singing birds of all birds surveyed during breeding bird point counts increased with level of radiation. We assumed that all singing birds were males, and this is likely to generally be the case (review in [36]). All singing individuals that were sexed using binoculars in the present study only revealed singing males. These findings have important implications for breeding bird surveys. Based on the present study we can conclude that previous estimates of species richness and abundance of birds reported by Møller and Mousseau [16]–[18], [20] for Chernobyl are likely to be over-estimates for areas with high levels of contamination. These relative estimates of density were based on the assumption of an even sex ratio, while in fact singing, unmated males were more frequent at high background radiation levels. Thus the negative effects of background radiation on abundance and species richness of breeding birds are likely to be stronger than previously thought. We can also conclude that the high frequency of singing birds in contaminated areas occurred despite the lower density of competitors in such areas, emphasizing the importance of song for mate attraction [12].

In conclusion, we have shown significant reductions in adult survival rates for a range of bird species in areas contaminated with low-dose radiation as reflected by skewed age ratios. Because adult female survival rate is differentially affected by radiation, we expected male-skewed tertiary sex ratios in contaminated areas, as we have documented. Independently, male birds sang disproportionately often in the most contaminated areas, as expected if there was a deficit of females, and if males sing in order to attract mates. There was no evidence consistent with the alternative hypothesis that females emigrated differentially from the most contaminated sites. These results suggest significant mortality costs of low-dose radiation with severe consequences for breeding populations of birds in vast areas of contamination in Ukraine, Russia and Belarus.

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